Objective: The purpose of this work is to assess the possible effect of aging on cVEMP in the Egyptian subjects to be compared with the international published response findings. Methods: After excluding subjects with previous history of dizziness, middle ear disorders or neuromuscular diseases, Forty subjects were equally divided into two age groups; group A: 20-40 years old (control group), group B: >60 years old (study group). VEMP was recorded for all subjects using tone burst 500 Hz stimuli at the threshold level and 95 dB n HL intensity level through air conduction stimulation. Results: There was a significant difference in the cVEMP response threshold (p< 0.001), P13 wave latency (p<0.001) between the two age groups. No significant difference was found between the right and left ears, N23 wave latency or in P13-N23 amplitude between the two groups. Conclusions: This study confirmed a significant increase in cVEMP thresholds and a significant prolongation of P13 latency with age. Normative age related data may be necessary to properly interpret cVEMP recordings when evaluating aging populations.

Cervical vestibular evoked myogenic potentials (cVEMPs) are reproducible, short-latency alternations in neck-muscle activity [measured in the sternocleidomastoid (SCM)] induced by intense sound stimuli (80–90 dBnHL) in participants regardless of their hearing status [1]. The cVEMP has been used clinically to test vestibular function in labyrinthine and central vestibular pathologies [2].

The Electromyography (EMG) activity is represented by a waveform with four peaks, which are characterized according to their latencies and polarities as P13, N23, P34, and N44 ([Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7]). The clinical usefulness of the last two peaks is limited, because they are present only in about 60% of healthy individuals and probably originate from cochlear afferents [3].{Figure 1}{Figure 2}{Figure 3}{Figure 4}{Figure 5}{Figure 6}{Figure 7}

A range of acceptable latencies of the PI and NII waveforms based on published age-appropriate ranges are as follows: PI, 8.5–14 ms and NII, 15–23 ms [4]. The mean latencies of first positive (P13) and first negative (N23) potentials in healthy individuals were 12.45±1.9 and 20.8±3.5 ms, respectively. The median latencies of these two potentials were 12.1 and 19.3 ms, respectively [5].

A significant delay in peak latencies is pathological. As the peak latency of P13 shows better reproducibility than that of N23, the peak latency of P13 is more available clinically. P13 latency is superior to N23 latency in evaluating the prolonged latencies of VEMP. Prolonged latencies are signs of retrolabyrinthine or central disorders [6].

Amplitude

The most reliable measure of the cVEMP response is the amplitude [7]. cVEMP amplitude is influenced by the tonic SCM muscle activation. There is a linear relation between the amplitudes of P13–N23 and the mean level of rectified electromyography response [3]. The amplitude of P13 increased with increasing stimulus intensity [3]. Ochi and Ohashi [8] concluded that amplitudes are not adequate for clinical practice due to the large SD of P13–N23 amplitude.

Age-related structural and functional deterioration of sensory and motor mechanisms, especially of the vestibular system, is a leading cause of dizziness and imbalance in older adults. It is well established that older individuals with a history of imbalance and dizziness are at a higher risk for fall-related injuries, loss of independence, and even death, all depicting the importance of determining the effect of aging on the vestibular system [9].

The effect of age on VEMP responses has been consistently demonstrated across investigations, which showed a reduction in amplitude and an increase in threshold with increased age [10]. Earlier studies reported age-related changes in P1/N1 amplitudes [8],[11], with decreasing potentials after the sixth decade of life [12].

Because VEMPs could be induced by the inhibitory impulses for SCM muscle tension, the amplitude might be affected by the tension in the SCM muscle during the recording session. Moreover, they reported that the amplitude of the average responses increased in direct proportion to the mean level of tonic muscle activation during the recording period. There is also a significant correlation between the P13–N23 amplitude and average muscle tonus during the 20-ms period immediately before the onset of each click [13].

However, it is well known that VEMP amplitudes are linearly dependent on the tonic activity of the SCM [3],[14]. The age-related changes in P13–N23 amplitude might be affected by SCM muscle tonus; however, the age-related changes in SCM muscle tonus are unlikely to affect threshold. Consequently, it is impossible to attribute all age-related changes in VEMPs to changes in muscle tonus. Hence, it is suggested that decreased activity in the vestibular neural pathway rather than changes in muscle tonus is responsible for the correlation between age and the parameters of VEMPs [15]. This effect is possibly caused by the decrease in vestibular hair cells [6], scarpa’s ganglion cells, and cells of the vestibular brainstem [16] during the aging process.

The aim of this work was to assess the possible effect of aging on the cVEMP response in the Egyptian participants to be compared with international published response findings.

Patients and methods

This study was conducted on 40 individuals attending the Audiology Clinic in the Kasr Al-Ainy Hospital and ethically approved from the ethical committee, faculty of medicine Cairo university. The study was conducted during the period between October 2013 and September 2014. The participants were equally divided into two age groups (each group included 20 participants): group A included participants between 20 and 40 years of age (the control group), and group B included participants greater than 60 years (the study group).

All participants had normal audiological function, with no dizziness, vertigo, or postural instability, as well as no diabetes, hypertension, or neurological disease.

Cervical vestibular evoked myogenic potential recording

The electrodes were placed as follows: the active electrode on the middle of the SCM muscle of the tested side, the reference electrode fixed at the suprasternal notch, and the ground electrode was placed on the opposite SCM. The participant was instructed to tense the muscle by turning the chin over to the contralateral shoulder during runs of acoustic stimulation, and he or she was instructed to relax in between the runs to avoid fatigue. The average time for testing was 25 min.

The stimuli were short tone bursts (500 Hz, rise/fall time 2 ms, and plateau time 2 ms) presented through air conduction using headphone TDH 39 (Telephonics company 770 Park Ave Huntington, NY 11743 United States). The stimuli were presented monaurally at an intensity of 95 dBnHL for air conduction VEMP at a frequency of 5 Hz, in a descending manner of 5 dB until reaching threshold. At least 100 sweeps within the acceptance criteria were averaged and two trials of averaged signals were obtained at each intensity to ensure reproducibility. The time window for analysis was 50 ms. With a preamplifier of band-pass filter of 10–2000 Hz and amplification of 5000 times.

The response biphasic P13–N23 wave was defined as an initial positive polarity (P13), occurring at a latency of ∼13 ms after stimulation onset, and a subsequent negative polarity (N23) occurring at a latency nearly 23 ms after stimulation onset. When the biphasic P13–N23 was present, P13 and N23 latencies and peak-to-peak P13–N23 amplitude were assessed.

Results

The present study comprised 40 individuals equally divided into two age groups: group A, which included participants between 20 and 40 years of age, and group B, which included participants who were 60 years or older.

Their ages ranged from 20 to 70 years, with a mean age of 46.4±16.95 years. Group A included participants whose ages ranged from 20 to 40 years, with a mean age of 30.4±6.49, and group B included participants whose ages from 60 to 70 years, with a mean age of 62.4±2.89 ([Table 1]). Of the 40 studied participants, 23 (57%) were female and 17 (43%) were male.{Table 1}

The results revealed that the cVEMP threshold was significantly elevated with age (right P=0.015; left P=0.004). As regards latencies, P13 latency significantly delayed as age increased (right P=0.005; left P=0.028), whereas N23 latency showed no significant difference (right P=0.123; left P=0.137). Moreover, the amplitude showed no significant difference between the 2 groups (right P=0.801; left P=0.640). The results are illustrated in [Table 3].{Table 3}

Sex difference in group A

The mean VEMP threshold for men in group A (20–40 years) was found to be 83.50±5.30 dBHL, whereas for women it was 83.00±3.50 dBHL for the right ear. The mean VEMP threshold in the left ear for men was 86.50±4.12 dBHL, whereas for women it was 84.00±5.16 dBHL. No significant difference in VEMP threshold values was found between men and women for the right ear (P=0.806) and for the left ear (P=0.247).

The P13 latency in men was 12.77±3.23 ms, whereas in women it was 14.16±1.82 ms for the right ear, with a nonsignificant difference (P=0.252); the P13 values for the left ear was 13.65±3.15 ms and 15.49±1.95 ms in men and women, respectively, which was also nonsignificant (P=0.133).

The N23 latency values in the right ear for men and women were 21.73±4.33 and 22.31±2.19, respectively, with a nonsignificant difference (P=0.707), whereas the values in the left ear for men and women were 22.53±3.12 and 22.66±2.27, respectively, which is also nonsignificant (P=0.915).

P13–N23 amplitude values for men and women were 90.23±46.03 and 93.03±53.20 in the right ear, respectively, with a nonsignificant difference (P=0.901), whereas the values in the left ear were 106.96±63.42 and 81.18±37.79 for men and women, respectively, which is also nonsignificant (P=0.284). The results are demonstrated in [Table 4].{Table 4}

Vestibular evoked myogenic potentials parameter comparison between men and women in group B

On comparing different VEMP parameters between men and women in group B, we found that there was no significant difference as regards threshold in the right ear (P=0.412) and threshold in the left ear (P=0.630).

P13 latency was also found to be nonsignificant (P=0.412 and P=0.987 for the right and left ears, respectively). Moreover, N23 showed no significant difference (P=0.844 and P=0.755 for the right and left ears, respectively).

There was no significant difference as regards amplitude in the right ear (P=0.920) and amplitude in the left ear (P=0.893). The results are shown in [Table 5].{Table 5}

The results revealed that there was no significant relation between hearing level and different VEMP parameters [Table 6].{Table 6}

Discussion

The peripheral and central nervous system exhibit an age-related structural deterioration, which may be responsible for vestibular reflex deficits and dizziness in elderly [17].

VEMP testing is currently being utilized in the assessment of a variety of vestibular etiologies. The pathway of the VEMP response is projected to begin in the saccule and extend along the inferior branch of the vestibular nerve to the vestibular nuclei and project to motor neurons in the SCM muscle causing a release from the contracted state [3].

This study was conducted on 20 individuals between 60 and 70 years of age, with a mean age of 62.4±2.89 with different degrees of high-frequency sensorineural hearing loss (SNHL) (from mild to severe) and 20 younger adults aged 20–40 years with a mean age 30.4±6.49 with normal hearing levels as the control group.

Threshold

The results showed that cVEMP thresholds significantly elevated with an increase in age. These results are in agreement with those of Janky and Shepard [15], who found significant mean threshold differences with respect to age groups in response to 500 and 750 Hz tone burst stimuli and significant positive correlations between age and VEMP threshold in response to all tone burst stimuli. Similar results were obtained by Ochi et al. [13], who reported the effects of age on VEMP response in sixty healthy adults. Their study showed a significant positive correlation between age and VEMP threshold. Welgampola and Colebatch [18] investigated the influence of aging on the vestibulocollic reflex in response to click stimuli and demonstrated that VEMP thresholds increased as age increased.

The increase in VEMP threshold may be caused by age-related functional changes in the sensory and neural components involved in the projection of VEMP responses. Some investigators have reported that the number of primary vestibular neurons declines significantly and gradually with age [6] with a steep decrease after the age of 60 years. Tang et al. [16] found a significant decrease in neuronal number in the human vestibular nucleus with advanced age. Not only age-related neuronal loss in the vestibular ganglion and nucleus but also the decreased thickness of vestibular myelinated afferents has also been reported. In fact, aging may affect the VEMP response pathway from the saccule scarpa ganglion, the inferior vestibular nerve, the lateral vestibular nucleus, and the lateral vestibulospinal tract to the SCM muscle [9].

Latency

The present research demonstrated that P13 wave latency was significantly delayed as age increases ([Table 4]). This may be because the spread of central transmission and the time required to activate the vestibulocollic reflex that causes the cVEMP response changed as age increases.

Analysis of the data also indicated that there was no N23 wave latency difference between the control and study groups. The results of P13 latency behavior are in agreement with those of Lee et al. [19], who reported same conclusion as regards the latency of P13. Maleki et al. [9] also reported a significant difference in P1 wave latency between the two age groups (P<0.001). Moreover, the results of N23 latency in the present study are in agreement with those of Janky and Shepard [15], who reported no difference between age groups for N23 latency in response to click and tone burst stimuli.

Prolongation of P13 latency may be a more accurate marker of age-related degeneration compared with N23 latency prolongation [9]. Prolongation of latencies of both waves may be a more appropriate determinant of age-related degeneration compared with N23 latency prolongation alone [20].

These results, however, are in disagreement with those of Welgampola and Colebatch [18] and Su et al. [21], who reported no significant difference in P13 latency as related to age. However, Basta et al. [12] reported that there was no difference in either P13 or N23 latency measurements across age groups. Possible explanations for this discrepancy are differences in recording techniques, such as variations in stimuli rise/fall time, and filter setting.

Amplitude

This study showed no significant differences between the two groups as regards P13–N23 amplitude (Table and Figure), although the P13–N23 amplitude decreased with age. Earlier studies reported age-related changes in P13–N23 amplitude [10],[11],[13],[20],[22], with decreasing potentials after the sixth decade of life. This decrease may be caused by decreases in the number of vestibular hair cells [6], scarpa’s ganglion cells [16], and cells of the vestibular brainstem during the aging process. The vestibulocolic reflex, a part of the vestibular system, may also be affected by aging. Ochi and Ohashi [8] and Su et al. [20] reported a decrease in cervical muscle tonicity with aging. Akin et al. [14] findings also suggest that the decrement in cVEMP amplitude is related to both age-related changes in the vestibular system and age-related changes in the SCM muscle. There was a lack of a uniform means of SCM muscle contraction monitoring between these studies [10],[11]. Because the amplitude of the VEMP response is contingent upon the degree of SCM muscle contraction, VEMP requires strict supervision. Our research observation confirmed that women are more cooperative compared with men during testing.

There is also a significant correlation between the P13–N23 amplitude and average muscle tonus during the 20-ms period immediately before the onset of each click [8]. However, Basta et al. [12] reported no significant differences in overall muscle tonicity regardless of age coupled with decreased VEMP amplitudes, attributing the decreased VEMP amplitude to a decline in physiologic function.

Sex

In this study, there was no significant difference between men and women in all VEMP parameters ([Table 5] and [Table 6]). This is in agreement with the findings of Ochi et al. [13], who reported no sex-related differences in the VEMP. However, Lee et al. [19] found that latencies were more prolonged in women and amplitude was higher in women than in men. Basta et al. [12] also reported sex and age-related differences. These differences were related to both vestibular response time and greater female cooperation during the examination, leading to a shorter latency and larger amplitude in women than in men [12]. Further evaluation of sex-related changes would require a fuller explanation about the position of examination, as well as strict supervision. Our research observation confirmed that women are more cooperative compared with men during testing.

There was no significant relationship between hearing level and different VEMP parameters in the study groups ([Table 6]). This is in agreement with the findings of Sazgar et al. [5], who compared the results of VEMP outcome on 50 patients with SNHL with 32 normal hearing volunteers and found that no significant correlation exists between the two groups as regards P13 and N23 latencies. However, Tang et al. [16] observed a significant relation between hearing loss at high frequencies and reduced cVEMP amplitudes (or reduced saccular function) in individuals 60 years or older. Age and noise exposure were significantly associated with measures of both cochlear and saccular dysfunction.

Conclusion

The results of the present study showed that aging can influence the parameters of the cVEMP response.cVEMP threshold significantly increases with age.People who are 60 years or older have significantly prolonged cVEMP P13 latency; however, cVEMP N23 latency was not significantly delayed.cVEMP amplitude was not significantly affected by age.Sex has no role with respect to the studied cVEMP parameters.Effect of audiometric configuration in the form of high-frequency SNHL was of no role on the cVEMP studied parameters.

cVEMP abnormalities in healthy older adults indicated the sensitivity of this test in identifying the early signs of vestibular dysfunction.